Independent effects of seawater pH and high PCO2 on olfactory sensitivity in fish: possible role of carbonic anhydrase

Abstract

Ocean acidification may alter olfactory-driven behaviour in fish by direct effects on the peripheral olfactory system; olfactory sensitivity is reduced in CO2-acidified seawater. The current study tested whether this is due to elevated PCO2 or the consequent reduction in seawater pH and, if the former, investigate the possible involvement of carbonic anhydrase, the enzyme responsible for the hydration of CO2 and production of carbonic acid. Olfactory sensitivity to amino acids was assessed by extracellular multi-unit recording from the olfactory nerve of the gilthead seabream (Sparus auratus L,) in normal seawater (pH ∼8.2), and after acute exposure to acidified seawater (pH ∼7.7, but normal PCO2; ∼340 µatm) and high PCO2 seawater (∼1400 µatm) at normal pH (∼8.2). Reduced pH in the absence of elevated PCO2 caused reduction in olfactory sensitivity to L-serine, L-leucine, L-arginine and L-glutamine, but not L-glutamic acid. Increased PCO2 in the absence of changes in pH caused reduced olfactory sensitivity to L-serine, L-leucine and L-arginine, including increases in their thresholds of detection, but had no effect on sensitivity to L-glutamine and L-glutamic acid. Inclusion of 1 mM acetazolamide (a membrane-permeant inhibitor of carbonic anhydrase) in the seawater reversed the inhibition of olfactory sensitivity to L-serine caused by high PCO2. Ocean acidification may reduce olfactory sensitivity by reduction in seawater pH and intracellular pH (of olfactory receptor neurones); the former by reducing odorant-receptor affinity, and the latter by reducing the efficiency of olfactory transduction. The physiological role of carbonic anhydrase in the olfactory receptor neurones remains to be explored.

Integrated organismal responses induced by projected levels of CO2 and temperature exposures in the early life stages of lake sturgeon

“…Therefore, periods of high transient p CO 2 but low temperature could influence the fish energy budgets, with the potential for negative impacts on foraging and growth (Boisclair & Sirois, 1993; Strobbe et al., 2011). Increased p CO 2 may have led to reductions in the olfactory sensitivity of lake sturgeon directly and by lowering freshwater pH (Velez et al., 2021), providing a potential link between total distance moved and olfactory sensitivity. Marine acidification likely has inconsistent effects on fish behaviour (Clark et al., 2020), and our results support those observations in lake sturgeon.…”

Behavioural Stress Propagation in Benthic Invertebrates Caused by Acute pH Drop-Induced Metabolites

“…Behavioural effects triggered by lowered pH are known to occur in different taxonomic groups such as crustaceans (de la Haye et al, 2011), marine ragworms (Bond, 2018), and fish (Munday et al, 2009), although recent research debates both their ubiquitousness and effect size (Clark et al, 2020a;Clements et al, 2020a,b, but see Clark et al, 2020b;Munday et al, 2020;Williamson et al, 2021 for the importance of which comparisons are made). In addition, it should be mentioned that although there is little literature disentangling the behavioural effects of pH drop vs. high CO2, an increasing body of recent research evidenced the role of pH-dependent altered chemical communication (Roggatz et al, 2016;Schirrmacher et al, 2020;Porteus et al, 2021;Velez et al, 2021).…”